Ecological Stoichiometry for Parasitologists

Home , Ecological stoichiometry, Macroecology

Opinion

1, 2

Randall J. Bernot * and Robert Poulin

Ecological stoichiometry (ES) is an ecological theory used to study the imbal- Highlights

ances of chemical elements, ratios, and ﬂux rates among organisms and the ES uses the balance of multiple ele-

ments and energy in organisms and

environment to better understand nutrient cycling, energy ﬂow, and the role of

their environment to understand nutri-

organisms in ecosystems. Parasitologists can use this framework to study ent cycling and energy ﬂow in ecolo-

gical systems.

phenomena across biological scales from genomes to ecosystems. By using

the common currency of elemental ratios such as carbon:nitrogen:phosphorus,

ES is a powerful framework for para-

–

parasitologists are beginning to explicitly link parasite host interactions to sitologists because it uses a common

currency that cuts across biological

ecosystem dynamics. Thus, ecological stoichiometry provides a framework

scales from genes to ecosystems.

for studying the feedbacks of parasites on the environment as well as the

effects of the environment on parasites and disease. Parasitologists can use ES to answer

questions ranging from topics that

have already been well studied, but

Why Ecological Stoichiometry? from new angles, to new frontiers in

disease ecology and epidemiology.

Ecological stoichiometry (ES) (see Glossary) is a framework for understanding ecological

dynamics (i.e., the changing nature of ecological systems) by using ﬁrst principles of chemistry

and the balance among multiple elements and energy [1]. As a theory, ES has matured to help

provide predictions about cellular, organismal, evolutionary, and ecosystem dynamics across a

range of systems [2]. Parasitology is a ﬁeld that can beneﬁt from an ES approach by providing a

basis for directly linking parasites to the broader ecological systems in which they are

embedded, as well as understanding parasite–host interactions at multiple levels of organiza-

tion. By framing parasite–host interactions in elemental ratios, as ES does, parasitologists can

directly scale-up across biological levels by using the same metrics of nutrient cycling and

energy ﬂow as those used by ecosystem ecologists. Thus, key environmental drivers of

parasitism and the potentially important feedbacks of parasites on ecosystems can be better

understood using ES. In this Opinion article, we (i) give a brief primer on ES for parasitologists, (ii)

present a conceptual framework of ES that illustrates the potential ways in which parasitologists

can use ES, and (iii) outline ongoing and future questions that can be addressed with ES while

reviewing a handful of recent examples from the literature.

What Is Ecological Stoichiometry?

Stoichiometry is the study of patterns of mass balance in the chemical conversions of different

types of matter [3]. Many people are introduced to, and use, stoichiometry when balancing

chemical reactions in introductory chemistry classes. These principles of mass balance are also

widely used by ecologists to study nutrient cycling and energy ﬂow in natural systems [1,3].

Carbon, nitrogen, and phosphorus are the elements most studied using the ES framework as they

comprised the Redﬁeld ratio [4], and C can be a useful proxy for energy while N and P are often

Department of Biology, Ball State

limiting nutrients for organisms and ecosystems. Vannatta and Minchella [5] built a strong

University, Muncie, IN 47306, USA

frameworkonwhichtounderstandparasite effectsonecosystemnutrient cycling.This framework Department of Zoology, University of

Otago, Dunedin, New Zealand

involves focusing on one nutrient at a time and can be a starting point for incorporating multiple

nutrients and their ratios, as well as alterations in nutrient ﬂux rates associated with altered host

physiology and behavior. Additionally, other elements besides C, N, and P may be limiting in other *Correspondence:

cases and thus worthy of explicit attention in an ES framework. For example, potassium has been [email protected] (R.J. Bernot).

928 Trends in Parasitology, November 2018, Vol. 34, No. 11 https://doi.org/10.1016/j.pt.2018.07.008

linked to fungal epidemics [6], and iron has long been studied for its role in infectious disease [7]. Glossary

Theratios ofthese and other micronutrients may play a role in both host and parasite homeostasis. Connectance: in a food web,

connectance is the proportion of

realized feeding links out of all the

Many organisms are adapted to maintain a homeostasis of elements needed for growth and

possible feeding links.

reproduction, deviations from which reduce ﬁtness [8]. In other words, many animals need to obtain a

Consumer-driven nutrient

consistent ratio of essential nutrients from their food. When food nutrient ratios differ from the recycling (CNR): the feedback

consumer’s homeostatic needs, a nutritional imbalance may result where one or more elemental mechanism linking consumer

dynamics and producer nutritional

nutrients limit growth or impair ﬁtness. The animal then conserves the limiting nutrient while removing status.

excess nonlimiting nutrients (Figure 1). Thus, animals often release or regenerate (through excretion or

Ecological stoichiometry (ES): the

egestion) nutrient elements at ratios different from those at which they ingest, leading to differential balance of multiple chemical

elements during ecological nutrient availability in the environment [1]. These limitations can be predicted using the mass balance

interactions.

of the elements.

Food chain length: the number of

species encountered as energy or

The relative amounts of essential elements or their ratio can determine nutrient use and cycling nutrients move from plants to top

predators in a food web. The

rates rather than their absolute amounts. In turn, differential nutrient regeneration at one trophic

number of links between the base of

level can affect other trophic levels and the broader ecosystem processes of nutrient cycling

the web and the top predator.

and energy ﬂow [3]. Importantly, ES has provided insights into large-scale biogeochemical

Growth rate hypothesis (GRH):

couplings of organisms at the ecosystem scale [9] while also guiding questions at the genomic differences in organismal C:N:P

ratios are caused by differential

and cellular end of the biological scale (reviewed in [1]). For example, freshwater snails

allocations to RNA necessary to

exacerbated phosphorus limitation in a stream ecosystem through high N:P excretion ratios

meet protein synthesis demands of

(i.e., less P per unit N) of individual snails, thus linking individual elemental use and ecosystem rapid biomass growth and

elemental cycling [10]. At the genomic scale, the elemental content of proteins is a function of development.

Homeostasis: maintenance of

the level of their encoding genes such that proteins associated with highly expressed genes in

constant internal conditions in the

plants are low in nitrogen compared to proteins encoded by low-expression genes [11].

face of externally imposed variation.

Consumer-driven nutrient recycling (CNR) [12,13], threshold elemental ratios (TERs) Metabolic theory of ecology

[14], and the growth rate hypothesis (GRH) [15] have all developed as key ecological (MTE): the fundamental biological

rate that governs most patterns in

concepts through ES [16]. More recently, efforts to understand the evolutionary dynamics

ecology is organism metabolic rate.

of stoichiometric traits have further expanded the scope of ES as a theory [2]. For example,

This theory is based on relationships

ﬁ

populations of rotifers fed P-de cient algal diets rapidly adapted to P-limiting conditions in among metabolic rate, body size,

and temperature.

which they had greater ﬁtness compared to individuals from populations on P-rich diets [17].

Nestedness: in a food web, the

Ecological stoichiometric approaches have been primarily developed in aquatic systems, while

degree to which species with few

the analogous framework of nutritional geometry (NG), which also centers on organismal

links are a subset of the links of

homeostasis and functionally relevant biochemical currencies, has matured from behavioral other species, rather than a different

set of links.

ecology and terrestrial insect ecology [16]. Additionally, the metabolic theory of ecology

Nutritional geometry (NG):

(MTE), which uses energy as a currency that scales across biological levels, has a number of

framework of nutritional ecology

common assumptions and goals as ES and NG [18–21]. Current efforts are underway to

linking animal physiology, behavior,

synthesize these frameworks to potentially arrive at a powerful perspective to link organisms and demography with macronutrients

and micronutrients such as

with their environment via the common currencies of materials and energy at many levels of

carbohydrates, lipids, and proteins.

biological organization [16]. These theories have not been developed using parasites, but we

Redﬁeld ratio: the atomic ratio of

contend that using parasites and their hosts to test hypotheses within these frameworks will C, N, and P found in ocean plankton

reﬁne and inform general ecological theory and advance parasitology. Many opportunities exist (C:N:P = 117:14:1). Named after

Alfred C. Redﬁeld who ﬁrst described

to not only test hypotheses from these theories using parasite systems, but to also inform more

the ratio.

traditional epidemiological approaches to parasitology and disease ecology. Thus, we can look

Threshold elemental ratios

at traditional parasitology through a new lens or from a slightly different angle [22]. Here, we (TERs): the nutrient ratio of an

’

focus on ES because it reduces the biochemicals of NG and MTE to elements and ratios of organism s food where that organism

switches from limitation by one of

elements (C:N:P) that are common currencies at all scales of biological organization.

these elements to limitation by

another.

An Ecological Stoichiometry Framework for Parasitology

Parasites, by deﬁnition, obtain energy and nutrients from their hosts. Thus, we can study the

effects of parasites on their hosts from the ES standpoint using the parasite as the consumer

Trends in Parasitology, November 2018, Vol. 34, No. 11 929

(A) Figure 1. Conceptual Diagrams (A)

Snail Representing the General Concept

of Nutrient Cycling through a

30N:1P

Resource and Snail Consumer,

and (B) How the Balance of N:P

30N:1P May Shift among a Resource, Snail

Consumer, and Trematode (Snail

Parasite) within the Snail (Data from

[15]). A freshwater snail’s resource often

Resource include periphyton, which is a complex of

algae, bacteria, and fungi. The nitrogen

30N:1P (N) and phosphorus (P) content of this

resource can vary and depends on nutri-

Parasite ent availability in the environment. The N

and P ratio (N:P) of the snail body is

20N:1P

(B) relatively homeostatic. When snails ingest

resources with nonhomeostatic N or P

content, this imbalance results in differ-

Snail ential N:P regeneration (excretion and

egestion) by the snail. 30N:1P

40N:1P

Resource

30N:1P

and the host as the resource (Figure 1). We can then link processes at multiple biological levels,

from the cellular to the individual to the ecosystem, because of the common currencies of

nutrient elemental content and ﬂux. At the individual level, many animals maintain a homeostatic

ratio of C:N:P or at least N and P [1]. Parasites may have different C:N:P requirements than their

hosts, creating a potential imbalance in homeostatic needs between consumer and resource

[23,24]. Indeed, the extent of the mismatch between host and parasite elemental ratios may

contribute to parasite virulence. Anthropogenic nutrient enrichment could possibly exacerbate

this mismatch if parasites can steal nutritional elements before they are used by the host for

immune defense or other functions [24]. While the concepts of nutrient limitation [25] and

nutrient eutrophication [26] on parasite dynamics have been studied, explicitly incorporating

multiple elements that feedback into the environment is the basis for ES and we argue will lead

to a fuller understanding of the role of parasites in ecosystems.

At the cellular and tissue levels, different tissues within a single organism often exhibit differ-

ences in elemental content. For example, the gonads of freshwater snails in the genus Physa

contain a lower N:P ratio compared to the head or foot tissue [23]. Trematodes that target

Physa gonads contained similar P content and N:P ratios as host gonads. Thus, parasites that

infect speciﬁc host tissues may have evolved to feed on tissues that meet their stoichiometric

homeostatic needs. Conversely, these parasites may have evolved homeostatic needs that

match those of the host tissue they exploit. Comparative ES studies of related parasite taxa that

differ in the host tissue they infect may help to resolve the forces driving the evolution of parasite

tissue speciﬁcity. In addition, ES may shed new light on the extent to which certain parasites

truly are parasites. For instance, gut-dwelling tapeworms and acanthocephalans, which have

930 Trends in Parasitology, November 2018, Vol. 34, No. 11

no mouth or gut and absorb food through their external surfaces, may follow more closely to the

stoichiometry of the food digested by their host that that of host tissues; the degree to which

they compete with the host, rather than feed on it, could be resolved by ES.

The advantages of using ES as a framework for addressing parasitology questions include all

the reasons that ecologists use it, and it also provides a straightforward framework for studying

how parasites affect ecosystems by using the same ﬁrst principles, elements, and rate

dynamics that ecosystem ecologists measure. The indirect effects of parasites on communities

have been studied in a phenomenological manner where a parasite affects a host or a set of

hosts and the net change in host behavior, life history, morphology, etc. cascades through the

community [27–29]. For example, trematode-infected freshwater snails grazed more rapidly

than other snails, resulting in a change in algal communities presumably due to the change in

grazing pressure [28]. Wood et al. [30] found that marine snails graze more slowly when they are

infected by trematodes, this also resulting in an effect on macroalgal communities. While both

of these studies found a link between parasite-altered behaviors and the broader ecological

community, neither used the common currency of nutrients to more directly link snail physiol-

ogy, behavior, and ecosystems. Conversely, the environmental drivers of parasite prevalence

and intensity are studied from a disease triangle framework by studying how the environment

affects both the parasite and the host [31], and increasingly from a community ecology angle

[32]. For example, the studies reviewed in Johnson et al. [32] aim to understand the environ-

mental factors associated with disease. An ES approach allows us to account for the feedbacks

of disease on the environment. Both of these approaches are somewhat limited in that

individual traits and community attributes are measured in many different units and currencies,

making emergent patterns and phenomena across systems difﬁcult to detect.

ES can be used to make clear hypotheses and predictions that more succinctly link feedbacks of

parasites on ecosystems. For example, a handful of recent studies have used ES to link the effects

of parasites on host nutrient regeneration. Bernot [23] measured the changes in nitrogen and

phosphorus excretion and egestion by a freshwater snail due to infection by a castrating trema-

tode that absorbed phosphorus at a faster rate than the host needed for growth. The result was

that infected snails excreted phosphorus at a slower rate than uninfected snails, thereby exacer-

bating phosphorus limitation in the system. Additionally, infected snails fed phosphorus-deﬁcit

food shed fewer trematode cercariae presumably due to less phosphorus available to the parasite

via its host.Different effects of trematodes onotherfreshwatersnails includefaster metabolicrates

that can inﬂuence nutrient cycling rates [33]. Mischler et al. [34] focused on changes in nitrogen

excretion by infected snails and extended these organismal-level parasite effects to whole-lake

ecosystems. In this case, trematodes caused snails to excrete nitrogen more rapidly, thereby

altering nitrogen cycling atthe pondlevel. Similarly,freshwatercrustaceannutrient recycling isalso

affected by parasites [35,36]. These studies have followed the traditional use of ES in aquatic

systems. Future studies can address whether the effects of parasites’ feedback to nutrient pools

and ﬂuxes in terrestrial and marine ecosystems, particularly where keystone species experience

high infection prevalence and altered host stoichiometry, is likely to have large cumulative effects

[5]. Studies in other systems have already taken an ES approach in weevil–tree [37], and fungus–

cyanobacterium [38] dynamics. In these cases, limiting nutrients were studied as limitations on

parasite success. Detailed elemental contents of some terrestrial organisms, like insects, are

already well documented [39], providing the basis for fruitful research using an ES approach.

Additionally, while more studies are including parasitesin food webs [40,41], ES can link food-web

metrics like connectance, nestedness, and food chain length to functional components of

empirical ecosystems like nutrient pools, nutrient ﬂuxes, and trophic efﬁciency [42]. Similarly, ES

can also be used to make clear hypotheses and predictions about how ecosystem and

Trends in Parasitology, November 2018, Vol. 34, No. 11 931

community-level process affect parasites and their hosts [43,44]. For instance, in a P-limited Outstanding Questions

ecosystem, a parasite may not be able to acquire sufﬁcient P from its host, reducing its ﬁtness, the How does the environment limit or not

limit epidemics? Is there a nutrient

ﬁtness of its host, or both.

threshold (in environment or host)

above which triggers an epidemic (or

below which keeps disease/parasite

Concluding Remarks

rare)?

In conclusion, ES uses the conservation of matter of essential nutrients such as C, N, and P to

understand pools and ﬂuxes of nutrients involved in interactions across all biological scales. For

How do parasite effects on hosts feed-

–

parasitology, using common nutrient currencies such as N:P can help to frame parasite host back to affect communities and

ecosystems?

interactions at multiple levels, including the ecosystem level where current disease ecology and

parasite ecology efforts are heading. We contend that ES provides a fruitful framework to ask

How and why do parasites affect host

many parasitology questions ranging from topics that have already been well studied to new

diet and allocation of limiting nutrients

frontiers in disease ecology and epidemiology (see Outstanding Questions).

to immune system function (produc-

tion of cells, function of cells, etc.)?

Of particular importance and priority should be the use of ES to better standardize effects and

Are there other limiting elements to

phenomena across scales from parasites to ecosystems. For example, asking whether

parasites or their hosts? Calcium?

nutrients in the environment limit or promote epidemics, and then whether the effects of an

Iron?

epidemic have reciprocal effects on the environment can be asked by following multiple

elements through pools of ecosystem compartments. The elements that are followed through

Are elements limiting or are larger nutri-

the ecosystem do not need to be the traditional C, N, or P, but could also include elements like tional compounds (lipids, proteins,

carbohydrates, etc.) more important

calcium, that limits host ﬁtness, or iron, that may limit parasite ﬁtness. This approach offers the

in affecting hosts and/or their

advantage of explicitly accounting for feedbacks of elements into and out of different organisms

parasites?

while using the measures and currency of ecosystem ecologists. Experimental studies where

key nutrient limitations are introduced and then followed through hosts, parasites, food webs, What are the physiological effects of

and ecosystems can inform broader ﬁeld studies of nutrient cycling in ecosystems differing in resource limitation on hosts and their

parasites? Do parasites amplify the

parasite diversity or prevalence.

negative effects of resource limitation?

Additionally, at an organismal level, the physiological effects of resource limitation on hosts and

Do parasites alter host elemental

their parasites can be studied within an ES framework. Do parasites amplify the negative effects composition?

of resource limitation? Do limiting nutrients affect host immune system function (production of

cells, function of cells, etc.)? The balance of key elements can be used to predict and potentially Do parasites affect the rates or ratios of

excreted or egested elements from

weaken the effects of parasites on their hosts.

hosts?

Acknowledgments Do parasites affect the point at which

nutrients become toxic to a host?

We thank the Evolutionary and Ecological Parasitology Research Group at the University of Otago for intellectual feedback,

the Department of Zoology at the University of Otago for hosting R.J. Bernot, and Melody Bernot, Noah Bernot, and Lillian

Does parasite prevalence and diversity

Bernot for writing support to R.J. Bernot. We also thank the Ball State University Sponsored Programs Administration

affect ecosystem function and trophic

ASPiRE program for funding.

efﬁciency through altered nutrient

cycling or limitation?

References

1. Hessen, D.O. et al. (2013) Ecological stoichiometry: an elemen- 6. Civitello, D.J. et al. (2013) Potassium stimulates fungal epidemics

tary approach using basic principles. Limnol. Oceanogr. 58, in a freshwater invertebrate. Ecology 94, 380–388

2219–2236

7. Weinberg, E.D. (1971) Roles of iron in host–parasite interactions.

2. Leal, M.C. et al. (2017) The ecology and evolution of stoichiomet- J. Infect. Dis. 124, 401–410

ric phenotypes. Trends Ecol. Evol. 32, 108–117

8. Persson, J. et al. (2010) To be or not to be what you eat:

3. Sterner, R.W. and Elser, J.J. (2002) Ecological Stoichiometry: The regulation of stoichiometric homeostasis among autotrophs

Biology of Elements from Molecules to the Biosphere, Princeton and heterotrophs. Oikos 119, 741–751

University Press

9. Vanni, M.J. (2002) Nutrient scycling by animals in freshwater

4. Redﬁeld, A.C. et al. (1963) The inﬂuence of organisms on the ecosystem. Annu. Rev. Ecol. Syst. 33, 341–370

composition of seawater. In The Sea (Hill, N.M., ed.), pp. 26–77,

10. Grifﬁths, N.A. and Hill, W.R. (2014) Temporal variation in the

Interscience

importance of a dominant consumer to stream nutrient cycling.

5. Vannatta, J.T. and Minchella, D.J. (2018) Parasites and their Ecosystems 17, 1169–1185

impact on ecosystem nutrient cycling. Trends Parasitol. 34,

452–455

932 Trends in Parasitology, November 2018, Vol. 34, No. 11

11. Elser, J.J. et al. (2011) Stoichiogenomics: the evolutionary ecol- 28. Bernot, R.J. and Lamberti, G.A. (2008) Indirect effects of a

ogy of macromolecular elemental composition. Trends Ecol. Evol. parasite on a benthic community: an experiment with trematodes,

26, 38–44 snails, and periphyton. Freshw. Biol. 53, 322–329

12. Evans-White, M.A. and Lamberti, G.A. (2006) Stoichiometry of 29. Raffel, T.R. et al. (2010) Parasitism in a community context: trait-

consumer-driven nutrient recycling across nutrient regimes in mediated interactions with competition and predation. Ecology

streams. Ecol. Lett. 9, 1186–1197 91, 1900–1907

13. Atkinson, C.L. et al. (2017) Consumer-driven nutrient dynamics in 30. Wood, C.L. et al. (2007) Parasites alter community structure.

freshwater ecosystems: from individuals to ecosystems. Biol. Proc. Natl. Acad. Sci. U. S. A. 104, 9335–9339

Rev. 92, 2003–2023

31. Hudson, P.J. et al. (2002) Ecology of Wildlife Diseases, Oxford

14. Frost, P.C. et al. (2006) Threshold elemental ratios of carbon and University Press

phosphorus in aquatic consumers. Ecol. Lett. 9, 774–779

32. Johnson, P.T.J. et al. (2015) Why infectious disease research

15. Elser, J. et al. (2008) Biological stoichiometry from genes to needs community ecology. Science 349, 1259504

ecosystems. Ecol. Lett. 3, 540–550

33. Chodkowski, N. and Bernot, R.J. (2017) Parasite and host ele-

16. Sperﬁeld, E. et al. (2017) Bridging ecological stoichiometry and mental content and parasite effects on host nutrient excretion and

nutritional geometry with homeostasis concepts and integrative metabolic rate. Ecol. Evol. 7, 5901–5908

models of organism nutrition. Funct. Ecol. 31, 286–296

34. Mischler, J. et al. (2016) Parasite infection alters nitrogen cycling

17. Declerck, S.A.J. et al. (2015) Rapid adaptation of herbivore con- at the ecosystem scale. J. Anim. Ecol. 85, 817–828

sumers to nutrient limitation: eco-evolutionary feedback to popula-

35. Narr, C.F. and Frost, P.C. (2015) Does infection tilt the scales?

tion demography and resource control. Ecol. Lett. 18, 553–562

Disease effects on the mass balance of an invertebrate nutrient

18. Allen, A.P. and Gillooly, J.F. (2009) Towards an integration of recycler. Oecologia 179, 969–979

ecological stoichiometry and the metabolic theory of ecology to

36. Narr, C.F. and Frost, P.C. (2016) Exploited and excreting: parasite

better understand nutrient cycling. Ecol. Lett. 12, 369–384

type affects host nutrient recycling. Ecology 97, 2012–2020

19. Hechinger, R.F. (2013) A metabolic and body-size scaling frame-

37. Ji, H. et al. (2017) Elemental stochiometry and compositions of

work for parasite within-host abundance, biomass, and energy

weevil larvae and two acorn hosts under natural phosphorus

ﬂux. Am. Nat. 182, 234–248

variation. Sci. Rep. 7, 45810

20. Ott, D. et al. (2014) Unifying elemental stoichiometry and meta-

38. Frenken, T. et al. (2017) Changes in N:P supply ratios affect the

bolic theory in predicting species abundances. Ecol. Lett. 17,

ecological stoichiometry of a toxic cyanobacterium and its fungal

1247–1256

parasite. Front. Microbiol. 8, 1015

21. Lagrue, C. et al. (2015) Parasitism alters three power laws of

39. Boswell, A.W. et al. (2008) The relationship between body mass

scaling in a metazoan community: Taylor’s law, density-mass

and elemental composition in nymphs of the grasshopper

allometry, and variance-mass allometry. Proc. Natl. Acad. Sci.

Schistocerca americana. J. Orthoptera Res. 17, 307–313

U. S. A. 112, 1791–1796

40. Lafferty, K.D. et al. (2008) Parasites in food webs: the ultimate

22. Stephens, P.R. et al. (2016) The macroecology of infectious

missing links. Ecol. Lett. 11, 533–546

diseases: a new perspective on global-scale drivers of pathogen

41. Selakovic, S. et al. (2014) Infectious disease agents mediate

distributions and impacts. Ecol. Lett. 19, 1159–1171

interaction in food webs and ecosystems. Proc. R. Soc. B

23. Bernot, R.J. (2013) Parasite host elemental content and the

281, 20132709

effects of a parasite on host consumer-driven nutrient recycling.

42. Thieltges, D.W. and Poulin, R. (2016) Food-web-based compari-

Freshw. Sci. 32, 299–308

son of the drivers of helminth parasite species richness in coastal

24. Aalto, S.L. et al. (2015) A three-way perspective of stoichiometric

ﬁsh and bird deﬁnitive hosts. Mar. Ecol. Prog. Ser. 545, 9–19

changes on host-parasite interactions. Trends Parasitol. 31,

43. Preston, D.L. et al. (2016) Disease ecology meets ecosystem

333–340

science. Ecosystems 19, 737–748

25. Penczykowski, R.M. et al. (2014) When bad food is good: poor

44. Sanders, A.J. and Taylor, B.W. (2018) Using ecological stoichi-

resource quality lowers transmission potential by changing for-

ometry to understand and predict infectious diseases. Oikos

aging behavior. Funct. Ecol. 28, 1245–1255

Published online May 29, 2018. http://dx.doi.org/10.1111/

ﬂ

26. Budria, A. (2017) Beyond troubled waters: the in uence of eutro- oik.05418

phication on host-parasite interactions. Funct. Ecol. 31,

1348–1358

27. Mouritsen, K.M. and Poulin, R. (2005) Parasites boost biodiversity

and change animal community structure by trait-mediated indi-

rect effects. Oikos 108, 344–350

Trends in Parasitology, November 2018, Vol. 34, No. 11 933